Stimulation Augments Spike Sequence Replay and Memory Consolidation during Slow-Wave Sleep

被引:27
作者
Wei, Yina [1 ]
Krishnan, Giri P. [1 ]
Marshall, Lisa [2 ,3 ]
Martinetz, Thomas [4 ]
Bazhenov, Maxim [1 ]
机构
[1] Univ Calif San Diego, Dept Med, La Jolla, CA 92093 USA
[2] Univ Lubeck, Inst Expt & Clin Pharmacol & Toxicol, D-23562 Lubeck, Germany
[3] Univ Lubeck, Ctr Brain Behav & Metab, D-23562 Lubeck, Germany
[4] Univ Lubeck, Inst Neuro & Bioinformat, D-23562 Lubeck, Germany
基金
美国国家科学基金会; 美国国家卫生研究院;
关键词
improve memory; memory consolidation; sleep; slow-wave oscillations; stimulation; targeted memory reactivation; CLOSED-LOOP STIMULATION; PREFRONTAL CORTEX; VISUAL-CORTEX; OSCILLATIONS; REACTIVATION; MECHANISMS; MODEL; NEUROTRANSMITTER; PROMOTES; SPINDLES;
D O I
10.1523/JNEUROSCI.1427-19.2019
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Newly acquired memory traces are spontaneously reactivated during slow-wave sleep (SWS), leading to the consolidation of recent memories. Empirical studies found that sensory stimulation during SWS can selectively enhance memory consolidation with the effect depending on the phase of stimulation. In this new study, we aimed to understand the mechanisms behind the role of sensory stimulation on memory consolidation using computational models implementing effects of neuromodulators to simulate transitions between awake and SWS sleep, and synaptic plasticity to allow the change of synaptic connections due to the training in awake or replay during sleep. We found that when closed-loop stimulation was applied during the Down states of sleep slow oscillation, particularly right before the transition from Down to Up state, it significantly affected the spatiotemporal pattern of the slow waves and maximized memory replay. In contrast, when the stimulation was presented during the Up states, it did not have a significant impact on the slow waves or memory performance after sleep. For multiple memories trained in awake, presenting stimulation cues associated with specific memory trace could selectively augment replay and enhance consolidation of that memory and interfere with consolidation of the others (particularly weak) memories. Our study proposes a synaptic-level mechanism of how memory consolidation is affected by sensory stimulation during sleep.
引用
收藏
页码:811 / 824
页数:14
相关论文
共 53 条
[1]   Sleep Spindles in Humans: Insights from Intracranial EEG and Unit Recordings [J].
Andrillon, Thomas ;
Nir, Yuval ;
Staba, Richard J. ;
Ferrarelli, Fabio ;
Cirelli, Chiara ;
Tononi, Giulio ;
Fried, Itzhak .
JOURNAL OF NEUROSCIENCE, 2011, 31 (49) :17821-17834
[2]   Cued memory reactivation during sleep influences skill learning [J].
Antony, James W. ;
Gobel, Eric W. ;
O'Hare, Justin K. ;
Reber, Paul J. ;
Paller, Ken A. .
NATURE NEUROSCIENCE, 2012, 15 (08) :1114-+
[3]   Slow-Wave Sleep-Imposed Replay Modulates Both Strength and Precision of Memory [J].
Barnes, Dylan C. ;
Wilson, Donald A. .
JOURNAL OF NEUROSCIENCE, 2014, 34 (15) :5134-5142
[4]   Phase of Spontaneous Slow Oscillations during Sleep Influences Memory-Related Processing of Auditory Cues [J].
Batterink, Laura J. ;
Creery, Jessica D. ;
Paller, Ken A. .
JOURNAL OF NEUROSCIENCE, 2016, 36 (04) :1401-1409
[5]  
Bazhenov M, 2002, J NEUROSCI, V22, P8691
[6]   BRAIN POTENTIALS DURING SLEEP [J].
Blake, H. ;
Gerard, R. W. .
AMERICAN JOURNAL OF PHYSIOLOGY, 1937, 119 (04) :692-703
[7]   System consolidation of memory during sleep [J].
Born, Jan ;
Wilhelm, Ines .
PSYCHOLOGICAL RESEARCH-PSYCHOLOGISCHE FORSCHUNG, 2012, 76 (02) :192-203
[8]   Sleep Oscillations in the Thalamocortical System Induce Long-Term Neuronal Plasticity [J].
Chauvette, Sylvain ;
Seigneur, Josee ;
Timofeev, Igor .
NEURON, 2012, 75 (06) :1105-1113
[9]   Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation [J].
Chen, Jen-Yung ;
Chauvette, Sylvain ;
Skorheim, Steven ;
Timofeev, Igor ;
Bazhenov, Maxim .
JOURNAL OF PHYSIOLOGY-LONDON, 2012, 590 (16) :3987-4010
[10]   Cued Reactivation of Motor Learning during Sleep Leads to Overnight Changes in Functional Brain Activity and Connectivity [J].
Cousins, James N. ;
El-Deredy, Wael ;
Parkes, Laura M. ;
Hennies, Nora ;
Lewis, Penelope A. .
PLOS BIOLOGY, 2016, 14 (05)